PROC. ENTOMOL. SOC. WASH. 109(2), 2007, pp. 359-365 A NEW SPECIES OF BINODOXYS (HYMENOPTERA: BRACONIDAE: APHIDIINAE), PARASITOID OF THE SOYBEAN APHID, APHIS GLYCINES MATSUMURA, WITH COMMENTS ON BIOCONTROL K. S. Pike, P. Stary, M. J. Brewer, T. Noma, S. Langley, and M. Kaiser (KSP) Entomologist, Washington State University, Irrigated Agriculture Research WA and Extension Center, 24106 N. Bunn Road, Prosser, 99350, U.S.A. (e-mail: [email protected]); (PS) Entomologist, Institute ofEntomology, Academy of Sciences of the Czech Republic, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic; (MJB, TN) Entomologists; and (SL, MK) Research Assistants, Michigan State University, B18 Food Safety and Toxicology Building, East Lansing, MI 48824- 1302, U.S.A. — Abstract. Binodoxys kelloggensis Pike, Stary, and Brewer, n. sp. (Hymenoptera: Braconidae: Aphidiinae), is described and illustrated. This aphidiine parasitoid, found in southcentral Michigan, is considered a native species, reared from the exotic soybean aphid. Aphis glycines Matsumura, from naturally infested field soybeans and from aphid-infested potted soybeans placed outdoors among assorted plants. It is one of eight parasitoid species now known to attack A. glycines in North America. Key Words: parasitoid, aphidiine, Binodoxys, aphid. Aphis, soybean, new species, description A main listing of the aphidiine para- The new soybean aphid pest. Aphis sitoids in North America is provided in glycines Matsumura (Heimpel and Shelly the Catalog of Hymenoptera in America 2004, Ragsdale et al. 2004, Venette and North of Mexico (Marsh 1979). Re- Ragsdale 2004), which is rapidly expand- search undertaken in the Pacific North- ing its range, affords an opportunity to west (Pike et al. 2000) supplemented this examine the adaption of local and in- list substantially both in taxonomy and troduced parasitoids to the new invasive aphid host range information on the aphid, and to document the unfolding group. However, for much of North events much the same as was undertaken America, the faunal composition, host in North America for the Russian wheat range, and ecology ofthe aphidiines have aphid, Diuraphis noxia (Kurdjumov) Noma not been extensively explored. There is (Pike et al. 2000, et al. 2005). a lack of information on the adaptation From field studies on soybean aphids of local parasitoids to newly introduced in southcentral Michigan, a native, un- pest aphid species, and insufficient or described species ofBinodoxys Mackauer misleading information on the adapta- was discovered attacking the aphid. The tion of accidentally or purposely intro- new parasitoid species is herewith named duced exotic parasitoids to both native and described. Also provided is a com- and exotic host aphids. plete listing of all parasitoids, both — 360 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON native and introduced, that to date have Binodoxys kelloggensis Pike, Stary, and been documented to use soybean aphid Brewer, new species as a host in North America. (Figs. 1-8) The new parasitoid reared from A. — Material. Holotype 2 (whole mount, glycines was taken from naturally (1) dry): USA, Michigan, Kalamazoo Co., infested soybean field plots at the Michi- near Hickory Corners, Michigan State gan State University Entomology Farm University Kellogg Biological Station, (EF) at East Lansing, Michigan, and (2) Long-Term Ecological Research Plots naturally infested soybean field plots and W (N 42.4, 85.4), 8-Sep-2004, A. Costa- artificially infested potted soybeans magna collector. Reared from Aphis placed for a time in field plots ofassorted glycines Matsmura derived from a natu- plants at the Michigan State University- Kellogg Biological Station, Long-Term rally-infested field plot of soybeans Ecological Research plots (KBS) near (Glycine max). In the vicinity were 1- Hickory Corners, Michigan. Field expo- hectare blocks of alfalfa, clover, corn, sures ofpotted soybeans at KBS were in poplar, wheat, and mixed stands of or near blocks of alfalfa, corn, clover, clover, dogbane, goldenrod. Queen ann's poplar, soybean, wheat, and mixed lace, sumac, and timothy. Holotype de- stands of clover, dogbane, goldenrod. posited in the National Museum of Queen Ann's lace, sumac, and timothy. Natural Hisrtory, Smithsonian Institu- Collections were made by T. Noma, S. tion, Washington, DC (USNM). Langley, and M. Kaiser, unless otherwise Paratypes: 62 specimens, all from the indicated. Kellogg Biological Station, reared from A. glycines in August or September 2004. Parasitoids of Aphis glycines in Nine (4 ?, 5 c^^) were from the same Michigan rearings as the holotype, the remainder Aphelinidae were derived from A. glycines introduced and allowed to multiply on potted Aphelinus al—bipodus (Hayat and Fatima) soybeans placed outdoors in stands of Material. USA, Michigan, EF, 19- alfalfa, poplar, and mixed stands of Sep-2003; KBS, l-Aug-2003, 16-Jul & clover, dogbane, goldenrod. Queen 16-Aug-2004. T. Noma collector. Ann's lace, sumac, and timothy. Para- types deposited in part in collections of Aphelinus asychis (Walker) USNM (8 2, 8 S), Michigan State Material.—USA, Michigan, EF, 8- University, East Lansing (8 ?, 8 c^^), Aug-2003; 23-Aug & 13-Sep-2004; Washington State University, Prosser (12 KBS, l-Aug-2003; 16-Jul, 16-Aug & 7- 2.4 c^ ), and P. Stary, Czech Republic (9 Sep-2004. T. Noma collector. 2.5 S). Braconidae: Aphidiinae Diagnosis. Binodoxys kelloggensis is characterized by 11-segmented antenna, Aphidius colemani Viereck by characters on the petiole where the Material.—USA, Michigan, EF, 9-Jul- primary (= spiracular) and the second- 2003, 23-Aug-2004; KBS, 27-Jun, 1-Aug, ary tubercles are almost ofequal size and & 12-Sep-2003, 7-Sep-2004. T. Noma their mutual distance of separation is collector. distinctly shorter than the width across the primary tubercles. The prongs bear 2 Aphidius ervi Haliday long setae on the upper side and 6-9 long Material.—USA, Michigan, KBS, 16- setae on the lower side; upper and lower Aug & 7-Sep-2004. T. Noma collector. marginal setae are ofsimilar length; with VOLUME NUMBER 109, 2 361 Fig. 1-11. Various morphological features (illustrations not to same scale). 1-8, Binodoxys kelloggensis. 1, Head (a, tentorio-ocular distance; b, inter-tentorial distance; c, malar space; d, length of eye). 2, Antennal flagellomeres. 3, Mesonotum (setal number and arrangement shown on mesoscutum [medial-pleural region] and scutellum). 4, Forewing (e, length ofstigma; f, width ofstigma; g, Rl post- marginal vein (= metacarpus); h, RS vein (radial sector). 5, Propodeum. 6, Petiole. 7, Genitalia (i, length of ovipositor sheath; j, length of prong). 8, Prong apex (close-up). 9-11, B. carolinensis. 9, Petiole. 10, Genitalia. 11, Prong apex (close-up). 2 long simple apical setae on the upper on the upper side and 9 setae on the side. It is described from Aphis glycines lower side which are about half the from Michigan. length of the opposite upper setae; with Of the local native species, B. caroli- 2 long setae at the apex. Also, there are nensis (Smith 1944), described from some differences in characters of the Aphis sp. in North Carolina (Smith petiole and ovipositor between the tw—o 1944), seems to be the closest relative, species (Figs. 6-7, B. kelloggensis characterized as follows: Antenna 11- petiole and genitalia; Figs. 9-10 [illus- segmented. The prongs bear 5 long setae trated by Stary from a slide mounted 362 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON — paratype], B. caroluiensis petiole and (about 1/20) shorter than across second- genitalia). ary tubercles; feebly rugose with a short Certain exotic East Asian Binodoxys longitudinal carina in second third; with spp. (Stary et al. unpublished data), if sparse long setae near secondary tuber- established in North America as control cles. Genitalia (Figs. 7-8): Ovipositor agents of A. glycines, might also cause sheaths remarkably narrow in distal identification problems. Though the East portion and curved [compare B. kellog- Asian spp. are very similar to B. kellog- gensis (Fig. 7) with B. carolinensis gensis, they are distinguishable by char- (Fig. 10)]. Prongs relatively short and acters on the prongs which bear 4-5 long strong, slightly arcuate at apex; with 2 setae on the upper side, with the upper long setae on upper side; with 2 long setae being longer than the lower oppo- simple setae at apex; with 6-9 long setae site setae; also, characters on the petiole on lower side; length of upper side and are different. — lower side setae about equal. Etymology. The name of the new Color: Head dark brown, palpi brown. species is derived from the type location, Antenna brown, scape, pedicel and the Kellogg Biological Station near narrow base of Fl light brown. Meso- Hickory Corners, Michigan. The name soma dark brown. Wing venation is attributed to K. Pike, P. Stary and M. brown. Legs brown, narrow basal por- Brewer. — tion of tibiae light brown. Metasoma Description. Female. Head (Fig. 1): generally brown. Petiole light brown. Eyes medium-sized. Malar space equal to Basal spot at tergum 2 light brown. 1/4 ofeye length. Antenna 11-segmented. Ovipositor sheaths and prongs dark Flagellar segment 1 (= Fl) (Fig. 2, brown. Table 1) usually slightly >2.5 as long as Length ofbody: ca. 1.2 mm. wide, usually with 2 or 3 placodes, setae Male. Antenna 12-13 segmented. Col- semi-erect and equal to 1/3 of segment. oration similar to female. F2 (Fig. 2) about 0.8-0.9X Fl, approx- imately twice as long as broad, about 1/5 Diaeretiella rapae (MTntosh) thicker than Fl, with 4-5 placodes. F5 (Fig. 2) slightly wider than F2. Meso- Material.—USA, Michigan, EF, 17- Noma soma (Fig. 3): Mesoscutum with notauli Jun-2003. T. collector. distinct in ascendent portion, effaced on disc where traced by a few long setae. Lysiphlebus testaceipes (Cresson) Propodeum (Fig. 5) with a broad pen- Material.—USA, Michigan, EF, 8- tagonal areola, carinae distinct, with Aug & 19-Sep-2003, 21-Jun, 23-Aug & a few setae. Forewing (Fig. 4, Table 1): 13-Sep-2004; KBS, 27-Jun, 1-Aug & 12- Stigma triangular, slightly <3 times as Sep-2003, 16-Aug and 7-Sep-2004. T. long as broad, Rl (= metacarpus) Noma collector. shorter than stigma length by a factor of 0.4--0.7. RS three times as long as Praon sp. stigma width; lower marginal setae dis- Material.—USA, Michigan, EF, 21- tinctly longer than surface setae. Meta- Jun-2004; KBS, 12-Sep-2003. T. Noma sonia: Petiole (Fig. 6) about twice as long collector. as width across primary tubercles; dis- tance between primary (= spiracular) Discussion and secondary tubercles less than half width across primary tubercles; width Research on the adaptation of local across primary tubercles very slightly parasitoids is usually realized within the I VOLUME NUMBER 109, 2 363 Table 1. Feature measurements ()j.m), counts, and comparison of female and male Binodoxys kelloggensis (from paratype series, n = 21 females, n = 14 males). FemaleAvg. (range) Head Antenna flagellomeres Fl (length) F2 (length) F5 (length) Fl (width) F2 (width) F5 (width) Antennal placoids Fl (no.) F2 (no) F5 (no.) Eye (length) Malar space (length) Inter-tentorial distance Tentorio-ocular distance Wing Stigma (length) Stigma (width) Postmarginal vein (Rl) Mesoscutal pleural setae Propodeal setae, anterior area Petiole length width at spiracular tubercles (1°) width at secondary tubercles (2°) distance betw 1° and 2" tubercles Genitalia Ovipositor sheath (length) Prong (length) Prong lowerside setae (no.) Prong upperside setae (no.) Comparisons Malar space / eye Fl (length / width) F2 (length / width) F5 (length / width) F5/ F2 Petiole (length / width at 1° tubercle) 2° / 1° tubercle Stigma (length/width) Stigma / R 364 PROCEEDINGS OF THE ENTOMOLOGICAL SOCIETY OF WASHINGTON Aphis glycines, as a new invasive aphid highest number of parasitoid species pest in North America, tends to reflect among the subfamilies of aphids (Stary the case of D. noxia on small grains - and Rejmanek 1981, Potter and Hawkins inadvertent pest introduction, subse- 1998). The adaptation of local parasi- quent pest expansion, adaptation oflocal toids is also in agreement with the Rule parasitoids combined with foreign of Faunistic Complexes in the biological searches, importation, and establishment control of aphids (Stary 1968, 1970). of new exotic parasitoid species. The value of A. cdbipodus and A. The presented determinations, eight colemani as introduced exotics has in- parasitoids in total, are some of the first creased with their parasitization of two records of parasitization of A. glycines exotic aphid pests {D. noxia, A. glycines). by local or exotic established parasitoid A similar situation has developed with A. species in North America (see also ervi in Chile (Stary 1996), and with L. Nielsen and Hajek 2005). Aphelinus testaceipes in the Mediterranean region albipodus and ApJiidius colemani are of France (Stary et al. 1988), Portugal examples of exotic species. Aphidiiis (Cecilio 1994) and Spain (Michelena et colemani was introduced against Russian al. 1994). Such multilateral biocontrol wheat aphid and other aphids in North results in added economic savings which America and A. cdbipodus against Rus- unfortunately have not been evaluated. sian wheat aphid. Both are now estab- Aphis glycines, as an exotic, expanding lished in several states. In addition to the pest in North America, is to some extent original target pest aphids, they have a useful model to demonstrate and verify been found to utilize some alternate parasitoid dynamics relative to multiple aphids, including A. glycines. The ap- target and nontarget hosts, and their pearance ofy4. colemani on A. glycines as adapation to differing environments a biocontrol agent was somewhat pre- across areas of aphid expansion. dictable (see Lin and Ives 2003). Bino- doxys kelloggensis is apparently a native Acknowledgments species which has secondarily adapted to We express thanks to A. Costamagna the newly introduced soybean aphid. Its for aphid collections, G. Graffor clearing true native aphid hosts have not been and mounting specimens, and D. Allison determined, but probably they are in the for manuscript review and assistance in genus Aphis. At the type locality, where illustration formatting and slide labelling. a mix of plants exists, six local aphid The work was made possible with the species have been found {Acyrthosiphon support of Michigan State University, pisum (Harris), Aphis sp., Nearctaphis Washington State University, and the bakeri (Cowen), Rhopcdosiphum padi Academy of Sciences of the Czech Re- (L.), Therioaphis trifolii (Monell) and public. We specifically acknowledge Uroleucon ccdigatiim (Richards)], but Grant S5007102 and the Entomology none of these are directly linked with Institute project Z50070508 of the Czech the parasitoid to date. A number of other local aphidiines Academy of Sciences. parasitize various Aphis spp. and related Literature Cited groups, and we expect in time that some of these will adapt to the congeneric A. Cecilio, A. 1994. Faunistic evolution after the glycines. North America is rich in species introduction of Lysiphlehus testaceipes (Cres- son) (Hymenoptera: Aphidiidae) in Portugal, (see Pike et al. 2000) that utilize members and its importance for the control of aphids. of the genus Aphis. In general, the Boletin de Sanidad Vegetal - Plagas 20: 471- aphidine aphids are associated with the 476. VOLUME NUMBER 109. 2 365 Heimpel, G. E. andT. E. Shelly. 2004. Thesoybean nidae) parasitoid assemblages on aphids aphid: A review of its biology and manage- (Homoptera). Oecologia 116: 234-242. ment. Annals ofthe Entomological Society of Ragsdale, D. Q. W., D. J. Voegtlin, and R. J. America 97: 203. O'Neil. 2004. Soybean aphid biology in North Lin, L. A. and A. R. Ives. 2003. The effect of America. Annals ofthe Entomological Society parasitoid host-size preference on host popu- ofAmerica 97: 204-208. lation growth rates: an example of Aphidius Smith, C. F. 1944. The Aphidiinae of North colemani and Aphis glycines. 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